Specificity of filiform hair afferent synapses onto giant interneurons in Periplaneta americana: anatomy is not a sufficient determinant.
The synapses between the filiform hair sensory afferents and giant interneurons (GIs) 1-6 of embryonic and first instar cockroaches, Periplaneta americana, were used to investigate the role of neuronal anatomy in determining synaptic specificity. The pattern of afferent-to-GI synapses was first determined by intracellular recording of excitatory postsynaptic potentials (EPSPs). The lateral (L) axon synapses only with GIs 3, 4, and 6, while the medial (M) axon synapses with the contralateral dendrites of all six GIs but with the ipsilateral dendrites only of GIs 1, 2, and 4. The three-dimensional anatomy of the filiform afferents and GIs was determined by injection of cobalt. There is little anatomical segregation of the filiform afferents; consequently, there is no correlation between the anatomy of the GIs and their synaptic inputs. The M axon and ipsilateral GI3 were studied in more detail by light and electron microscopy. Despite the presence of an anterior M axon branch which loops around the ipsilateral GI3 neurite at a distance of 2 microns, no synapses are formed between them. This lack of synapses is not due to the presence of physical barriers. Investigation of filiform afferents and GIs in embryonic ganglia shows that at no stage are the afferents sufficiently separated for their anatomy to be an important factor in determining the specificity of the synaptic inputs of the GIs. It was postulated that two pairs of complementary cell surface labels would be sufficient to code for this specificity, and that, in GIs 3, 5, and 6, spatial differences in the expression of these labels allow the M axon to distinguish ipsilateral dendrites from contralateral.
Blagburn
J M
JM
Institute of Neurobiology, University of Puerto Rico Medical Sciences Campus, Old San Juan 00901.
Thompson
K S
KS
D000818:Animals; D005071:Evoked Potentials / Q000502:physiology; D007395:Interneurons / Q000648:ultrastructure*; D009475:Neurons, Afferent / Q000648:ultrastructure*; D010526:Periplaneta / Q000033:anatomy & histology*; D013569:Synapses / Q000648:ultrastructure*